Rapid evolution of the cerebellum in humans and other great apes Article Accepted Version Barton, R. A. and Venditti, C. (2014) Rapid evolution of the cerebellum in humans and other great apes. Current Biology, 24 (20). pp. 2440 2444. ISSN 0960 9822 doi: https://doi.org/10.1016/j.cub.2014.08.056 Available at http://centaur.reading.ac.uk/61349/ It is advisable to refer to the publisher s version if you intend to cite from the work. Published version at: http://dx.doi.org/10.1016/j.cub.2014.08.056 To link to this article DOI: http://dx.doi.org/10.1016/j.cub.2014.08.056 Publisher: Cell Press All outputs in CentAUR are protected by Intellectual Property Rights law, including copyright law. Copyright and IPR is retained by the creators or other copyright holders. Terms and conditions for use of this material are defined in the End User Agreement. www.reading.ac.uk/centaur CentAUR Central Archive at the University of Reading
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Rapid evolution of the cerebellum in humans and other great apes Robert A Barton 1,* and Chris Venditti 2* 1 Evolutionary Anthropology Research Group, Durham University, Durham DH1 3LE r.a.barton@durham.ac.uk, tel. +44(0) 191 3341603 2 School of Biological Sciences, University of Reading, Reading, RG6 6BX, UK., tel. +44 (0) 118 378 4683 * corresponding authors. Running title: cerebellum evolution in apes
Summary Using a method for detecting evolutionary rate changes along the branches of phylogenetic trees, we show that the cerebellum underwent rapid size increase throughout the evolution of apes, including humans, expanding significantly faster than predicted by the change in neocortex size. As a result, humans and other apes deviate significantly from the These results suggest that cerebellar specialization was a far more important component of human brain evolution than hitherto recognized, and that technical intelligence was likely to have been at least as important as social intelligence in human cognitive evolution. Given the role of the cerebellum in sensory-motor control and learning complex action sequences, cerebellar specialization is likely to have underpinned the evolution of humans advanced technological capacities, which in turn may have been a pre-adaptation for language.
β β β
Data and Phylogeny Data on cerebellum and neocortex volumes (mm 3 ) in anthropoid primates were collated from six primary sources. Mean species values were log-transformed prior to analysis. In addition, we obtained one data set on neocortical and cerebellar mass (g) one on volume of the cerebellar granule cell layer (μm3), and one on neuron numbers. These data and associated references are presented in Supplemental Table 1 and Supplemental Figure 1. For phylogenetic analyses (see below), we used the 10k Trees consensus primate phylogeny with GenBank species names [32]. The tree was pruned according to the species in our data set. Phylogenetic and Statistical Methods To determine the branch-wise rates of evolution separately for the cerebellum and neocortex, we used the Bayesian reversible-jump variable-rates model of trait evolution [33]. This model allows us to trace the evolutionary history of shifts in the rate and timing of evolution without specifying in advance where these events are located. To examine the cerebellum volume is the dependent variable and log neocortex volume is the independent variable. This allows us to estimate the rate of cerebellum evolution while accounting for the neocortex. For each analysis, over the course of one billion of iterations after convergence, sampling every 100,000 to ensure each subsequent sample is independent, we record for each branch in the tree what its mean rate is. These mean rates are then be used to scale the branches of
phylogenetic tree to produce a scaled tree that better represent the evolution of the morphological trait of interest (the scaled branches are plotted in figure to along with the untransformed branches in time). We repeated each of our analyses multiple times to ensure convergence was achieved. We reconstructed the ancestral states for each node in our tree while accounting for the rate variation revealed by the variable rates model of trait evolution (shown in Figure 1). Accounting for rate variation along the branches of the trees allows us to detect trends in size that would be opaque to other methods. We us BayesTraits following the protocol outlined in Organ et al [34] to impute the ancestral sizes as this approach has been show to outperform other methods for reconstruction ancestral states for continuously varying data [35]. This two stage Bayesian reconstruction methods first identifies the best fitting phylogenetic evolutionary model to the species data, then uses this model to infer unknown ancestral states at specified internal nodes in the tree we ran the MCMC chains to the same specifications as above and plot the means of the posterior distributions in Figure 1. We used Phylogenetic Least Squares (PGLS) [36-38] implemented in the R-package Caper (http://cran.r-project.org/web/packages/caper/vignettes/caper.pdf) to compute maximum likelihood (ML) parameter estimates for regressions and to test for significant differences between apes and other species while accounting for the shared ancestry implied by our phylogeny. In each regression the phylogenetic signal is estimated as the value of λ of the residuals, varying between 0 (where the data have no phylogenetic
structure) and 1 (where the best fit to the data is provided by a Brownian Motion model of trait evolution) [38], with variation at the tips proportional to the duration of common evolution [36-37]. The estimated ML value of λ is simultaneously estimated together with the other parameters in the model, thus controlling for phylogenetic signal in the data. Predicted values for an individual species based on the relationship between cerebellum and neocortex size can be tested using phylogenetic prediction, as outlined in Organ et al [34]
Arnold, C., L. J. Matthews, and C. L. Nunn. 2010. The 10kTrees Website: A New Online Resource for Primate Phylogeny. Evolutionary Anthropology 19:114-118. Venditti, C., Meade, A. and Pagel, M. (2011) Multiple routes to mammalian diversity. Nature, 479, 393-396. Pagel MD (1999) The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst Biol 48:612 622. Rohlf FJ (2001) Comparative methods for the analysis of continuous variables: Geometric interpretations. Evolution 55(11):2143 2160.
Freckleton RP, Harvey PH, Pagel MD (2002) Phylogenetic analysis and comparative data: A test and review of evidence. Am Nat 160(6):712 726.
Table 1: Branchwise increases in relative rates of cerebellum evolution within the ape clade (see text for explanation)
Log cerebellum volume (cm 3 ) 5 4 3 Log neocortex volume (cm 3 ) 6 5 4
Branch length scaled by rate 20 15 10 5 0 0 5 10 15 20 25 Branch length in time
Log cerebellum volume (cm 3 ) 5 4 3 2 3 4 5 6 Log neocortex volume (cm 3 )